Year-Round Bat Activity and Species Richness Near Temporary Ponds in the Mediterranean Region.

Mediterranean temporary ponds are recognized as conservation priority habitats that face anthropogenic threats and are important habitats for a number of aquatic and terrestrial animals and plants. Bats are a diverse group of animals that use ponds for drinking and feeding on emerging aquatic insects and terrestrial insects in the riparian zone. We investigated the importance of temporary ponds for bats in Greece by acoustically sampling bat community structures and activity at temporary ponds throughout the year. We sampled monthly, from 3 to 13 months in 2019-2020, at sites at the pond edge and approximately 150-300 m away from the edge, at four temporary ponds in northern and southern Greece. Our results confirm the importance of temporary ponds for bats as activity was recorded year-round and was high in all but the winter months. In general, the distance to the edge of the pond and the presence of water in the pond explained bat activity together with air temperature. Importantly, whether dry or not, all ponds supported bat activity, independent of their particular characteristics. This study highlights the urgent need for the conservation of temporary ponds, especially in areas with limited water availability.

Testosterone pulses paired with a location induce a place preference to the nest of a monogamous mouse under field conditions.

Changing social environments such as the birth of young or aggressive encounters present a need to adjust behavior. Previous research examined how long-term changes in steroid hormones mediate these adjustments. We tested the novel concept that the rewarding effects of transient testosterone pulses (T-pulses) in males after social encounters alter their spatial distribution on a territory. In free-living monogamous California mice (Peromyscus californicus), males administered three T-injections at the nest spent more time at the nest than males treated with placebo injections. This mimics T-induced place preferences in the laboratory. Female mates of T-treated males spent less time at the nest but the pair produced more vocalizations and call types than controls. Traditionally, transient T-changes were thought to have transient behavioral effects. Our work demonstrates that in the wild, when T-pulses occur in a salient context such as a territory, the behavioral effects last days after T-levels return to baseline.

The luxury effect beyond cities: bats respond to socioeconomic variation across landscapes.

BACKGROUND: The luxury effect describes the positive relationship between affluence and organism diversity or activity in urban ecosystems. Driven by human activities, the luxury effect can potentially be found at a broader scale across different landscapes. Previously, the luxury effect relationship has been established within a city for two bat species, the red bat (Lasiurus borealis) and the evening bat (Nycticeius humeralis). We examined landscape-scale patterns of bat activity distribution-using empirical data for seven bat species for the luxury effect. We also identified bat-land cover associations for each species. Across North Carolina, USA, we used the mobile transect survey protocol of the North American Monitoring Program to record bat activity at 43 sites from 2015 to 2018. We collected land cover and income data at our transect locations to construct generalized linear mixed models to identify bat-land cover and bat-income relationships. RESULTS: We found that across landscapes, activity of the red bat and the evening bat was positively correlated to income independent of land cover, consistent with previous single-city results. We found a negative relationship between hoary bat (Lasiurus cinereus) activity and income. All seven species had specific land cover associations. Additionally, we found a positive interaction term between income and evergreen forest for the red bat and a positive interaction term between income and woody wetland for hoary bat. CONCLUSIONS: Our results demonstrated that the luxury effect is an ecological pattern that can be found at a broad spatial scale across different landscapes. We highlight the need for multi-scale ecology studies to identify the mechanism(s) underlying the luxury effect and that the luxury effect could cause inequity in how people receive the ecosystem services provided by bats.

Rapid increases in bat activity and diversity after wetland construction in an urban ecosystem.

Wetland construction can mitigate the biodiversity and water quality losses associated with reduced natural wetland coverage. While beneficial effects of wetland construction for bats have been observed in natural and rural settings, the effects of wetland construction on bats in an urban ecosystem are less understood. We used passive acoustic monitoring to measure bat activity levels and diversity at two constructed wetlands and two control sites on the University of North Carolina Greensboro campus, in Greensboro, North Carolina, USA. We monitored all 4 sites before and after wetland construction. Pre-wetland construction, there were few differences in bat activity and community structure at our sites. After wetland construction, we observed greater activity, attributable to all species we recorded, at wetland sites compared to control sites. Species diversity and species richness were also higher at wetland sites compared to control sites. When comparing the same sites before and after wetland construction, both bat activity and species richness increased after construction, but the effects were seen in Winter and not Spring. Our results demonstrate that bats use constructed wetlands in urban ecosystems similarly to other habitat settings. Increases in bat activity, diversity, and species richness occurred within one year of wetland construction.

Separating the effects of water quality and urbanization on temperate insectivorous bats at the landscape scale.

Many local scale studies have shown that bats respond to water quality degradation or urbanization in a species-specific manner. However, few have separated the effects of urbanization versus water quality degradation on bats, in single city or single watershed case studies. Across North Carolina, USA, we used the standardized North American Bat Monitoring Program mobile transect protocol to survey bat activity in 2015 and 2016 at 41 sites. We collected statewide water quality and urban land cover data to disentangle the effects of urbanization and water quality degradation on bats at the landscape scale. We found that statewide, water quality degradation and urbanization were not correlated. We found that bats responded to water quality degradation and urbanization independently at the landscape scale. Eptesicus fuscus and Lasiurus cinereus negatively responded to water quality degradation. Lasiurus borealis and Perimyotis subflavus positively responded to water quality degradation. Lasionycteris noctivagans did not respond to water quality degradation but was more active in more urbanized areas. Tadarida brasiliensis positively responded to urbanization and was less active in areas with degraded water quality. We show that bat-water quality relationships found at the local scale are evident at a landscape scale. We confirm that bats are useful bioindicators for both urbanization and water quality degradation. We suggest that water quality can be used to predict the presence of bat species of conservation concern, such as P. subflavus, in areas where it has not been studied locally.

Winter Activity of Coastal Plain Populations of Bat Species Affected by White-Nose Syndrome and Wind Energy Facilities.

Across the entire distribution of a species, populations may have variable responses to environmental perturbations. Many bat species experience mortality in large portions of their range during hibernation and along migratory paths to and from wintering grounds, from White-nose syndrome (WNS) and wind energy development, respectively. In some areas, warm temperatures may allow bats to remain active through winter, thus decreasing their susceptibility to WNS and/or mortality associated with migration to wintering grounds. These areas could act as a refugia and be important for the persistence of local populations. To determine if warmer temperatures affect bat activity, we compared year-round activity of bat populations in the Coastal Plain and Piedmont of North Carolina, USA, two regions that differ in winter temperature. We established six recording stations, four along a 295-kilometer north-south transect in the Coastal Plain, and two in the Piedmont of North Carolina. We recorded bat activity over two years. We supplemented our recordings with mist-net data. Although bat activity was lower during winter at all sites, the odds of recording a bat during winter were higher at Coastal Plain sites when compared with Piedmont sites. Further, bats in the Piedmont had a lower level of winter activity compared to summer activity than bats in the Coastal Plain that had more similar levels of activity in the winter and summer. We found high bat species richness on the Coastal Plain in winter, with winter-active species including those known to hibernate throughout most of their range and others known to be long distance migrants. In particular, two species impacted by WNS, the northern long-eared bat (Myotis septentrionalis) and tricolored bat (Perimyotis subflavus), were present year round in the Coastal Plain. The tricolored bat was also present year-round in the Piedmont. In the Coastal Plain, the long distance migratory hoary bat (Lasiurus cinereus) was active in the winter but not present during the other seasons, and the long distance migratory silver-haired bat (Lasionycteris noctivagans) was active primarily in the winter, suggesting the Coastal Plain may be an overwintering ground for these two species. We suggest that the winter activity exhibited by populations of bats on the North Carolina Coastal Plain has important conservation implications and these populations should be carefully monitored and afforded protection.

Ultrasonic Vocalizations of Male Mice Differ among Species and Females Show Assortative Preferences for Male Calls.

Male house mice (Mus musculus) emit ultrasonic vocalizations (USVs) during courtship, which attract females, and we aimed to test whether females use these vocalizations for species or subspecies recognition of potential mates. We recorded courtship USVs of males from different Mus species, Mus musculus subspecies, and populations (F1 offspring of wild-caught Mus musculus musculus, Mus musculus domesticus (and F1 hybrid crosses), and Mus spicilegus), and we conducted playback experiments to measure female preferences for male USVs. Male vocalizations contained at least seven distinct syllable types, whose frequency of occurrence varied among species, subspecies, and populations. Detailed analyses of multiple common syllable types indicated that Mus musculus and Mus spicilegus could be discriminated based on spectral and temporal characteristics of their vocalizations, and populations of Mus musculus were also distinctive regardless of the classification model used. Females were able to discriminate USVs from different species, and showed assortative preferences for conspecific males. We found no evidence that females discriminate USVs of males from a different subspecies or separate populations of the same species, even though our spectral analyses identified acoustic features that differ between species, subspecies, and populations of the same species. Our results provide the first comparison of USVs between Mus species or between Mus musculus subspecies, and the first evidence that male USVs potentially facilitate species recognition.

Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse.

The steroid hormone testosterone (T) is a well-known mediator of male sexual behavior in vertebrates. However, less is known about T's rapid effects on sexual behavior, particularly those involving ultrasonic vocalizations (USVs), a mode of communication that can influence mate acquisition in rodents. Using the monogamous California mouse, Peromyscus californicus, we tested whether T rapidly alters male USV production by giving T or saline injections to non-paired (sexually naïve) males and paired (paternally experienced and pair-bonded) males immediately prior to a brief exposure to an unrelated, novel female. Among non-paired males, no differences in the total number of USVs were observed; however, T increased the proportion of simple sweeps produced. Among paired males, T decreased the number of USVs produced, and this change was driven by a reduction in simple sweeps. These results suggest a differential rapid effect of T pulses between non-paired and paired males upon exposure to a novel female. Additionally, we observed a positive correlation in the production of USVs made between males and novel females, and this relationship was altered by T. Given the importance of USVs in sexual communication, our study supports an essential concept of monogamy in that mate fidelity is reinforced by decreased responsiveness to prospective mates outside of the pair bond. The central mechanism in pair bonded males that decreases their responsiveness to novel females appears to be one that T can trigger. This is among the first studies to demonstrate that T can inhibit sexually related behaviors and do so rapidly.

Differences in ultrasonic vocalizations between wild and laboratory California mice (Peromyscus californicus).

BACKGROUND: Ultrasonic vocalizations (USVs) emitted by muroid rodents, including laboratory mice and rats, are used as phenotypic markers in behavioral assays and biomedical research. Interpretation of these USVs depends on understanding the significance of USV production by rodents in the wild. However, there has never been a study of muroid rodent ultrasound function in the wild and comparisons of USVs produced by wild and laboratory rodents are lacking to date. Here, we report the first comparison of wild and captive rodent USVs recorded from the same species, Peromyscus californicus. METHODOLOGY AND PRINCIPAL FINDINGS: We used standard ultrasound recording techniques to measure USVs from California mice in the laboratory (Peromyscus Genetic Stock Center, SC, USA) and the wild (Hastings Natural History Reserve, CA, USA). To determine which California mouse in the wild was vocalizing, we used a remote sensing method that used a 12-microphone acoustic localization array coupled with automated radio telemetry of all resident Peromyscus californicus in the area of the acoustic localization array. California mice in the laboratory and the wild produced the same types of USV motifs. However, wild California mice produced USVs that were 2-8 kHz higher in median frequency and significantly more variable in frequency than laboratory California mice. SIGNIFICANCE: The similarity in overall form of USVs from wild and laboratory California mice demonstrates that production of USVs by captive Peromyscus is not an artifact of captivity. Our study validates the widespread use of USVs in laboratory rodents as behavioral indicators but highlights that particular characteristics of laboratory USVs may not reflect natural conditions.

Influence of intensive pine management on Dipteran community structure in coastal North Carolina.

Intensive pine (Pinus spp.) management is a primary land use in the southeastern United States. In eastern North Carolina, intensively managed pine stands often occur on land previously ditched and drained. Because modification of natural vegetation and water sources are known to affect dipteran community structure, we studied effects of intensive pine management on abundance and diversity of dipteran families in the northern coastal plain of North Carolina during 2006 and 2007. We used malaise traps and emergence traps to sample different types of forest stands (n = 143 sample nights) and water sources (n = 147 sample nights) in a managed pine forest and a natural forested wetland. Cecidomyiids were more abundant in stands with canopy cover, chironomids were more abundant at edges between forested stands and open canopy stands, and chloropids were more abundant in open canopy stands. Families Ceratopogonidae, Dolichopodidae, Ephydridae, Muscidae, Psychodidae, and Tipulidae were more abundant in the natural forested wetland than in all types of modified water sources. Dipteran diversity and evenness were highest in stands with open canopy and at forest edges, and highest in the natural forested wetland. Unmanaged, natural stands on the intensively managed landscape did not support a higher abundance or diversity of dipteran families than intensively managed stands. Restoration of natural wetlands may increase dipteran diversity in unmanaged stands. Heliponds, a modified water source, supported a comparable dipteran abundance to that of the natural forested wetland. Increased numbers of heliponds may facilitate higher dipteran abundance in managed pine landscapes.

A genetic analysis of group movement in an isolated population of tree-roosting bats.

Group fission is an important dispersal mechanism for philopatric adults. In Cypress Hills Interprovincial Park, Saskatchewan, tree-roosting big brown bats (Eptesicus fuscus) exhibit fission-fusion roosting behaviour. During 2004-2007, the majority of females previously resident to roosting area 1 (RA1) moved to a new roosting area (RA4). We examined how genetic relationships, inferred from data for microsatellite loci and mitochondrial DNA, influenced new roost area (RA) selection during 2006 when colony members were split between the RAs. We found that females who moved to RA4 had higher average relatedness than those that remained in RA1. We found that nearly all females belonging to matrilines with high average relatedness moved to RA4 while females from matrilines with low average relatedness were split between the two RAs. These results suggest that closely related maternal kin preferentially move to new RAs. However, daily roosting preferences within a RA are not based on genetic relationships probably because daily roosting associations between kin and non-kin are used to ensure adequate roost group size. Studying the effects of kinship on the fission and movements of groups not only enhances our understanding of social behaviour and population genetics but also informs conservation decisions.

Production of ultrasonic vocalizations by Peromyscus mice in the wild.

BACKGROUND: There has been considerable research on rodent ultrasound in the laboratory and these sounds have been well quantified and characterized. Despite the value of research on ultrasound produced by mice in the lab, it is unclear if, and when, these sounds are produced in the wild, and how they function in natural habitats. RESULTS: We have made the first recordings of ultrasonic vocalizations produced by two free-living species of mice in the genus Peromyscus (P. californicus and P. boylii) on long term study grids in California. Over 6 nights, we recorded 65 unique ultrasonic vocalization phrases from Peromyscus. The ultrasonic vocalizations we recorded represent 7 different motifs. Within each motif, there was considerable variation in the acoustic characteristics suggesting individual and contextual variation in the production of ultrasound by these species. CONCLUSION: The discovery of the production of ultrasonic vocalizations by Peromyscus in the wild highlights an underappreciated component in the behavior of these model organisms. The ability to examine the production of ultrasonic vocalizations in the wild offers excellent opportunities to test hypotheses regarding the function of ultrasound produced by rodents in a natural context.